Global cancer statistics
Authors: D. M. Parkin, P. Pisani, J. Ferlay
Journal: CA A Cancer Journal for Clinicians (1999)

A choice of statistics is available for measuring the impact of cancer on the community. One should think about the exact purpose of the exercise and what comparisons are required before deciding which statistics are most appropriate. Incidence is the number of new cases occurring. It can be expressed as an absolute number of cases per year (which tells us about the volume of new patients presenting for treatment) or as a rate per 100,000 persons per year. The latter approximates the average risk of developing a cancer, which is particularly useful in making comparisons among populations (countries, ethnic groups, or different periods within a country, for example). Mortality is the number of deaths occurring, and the mortality rate is the number of deaths per 100,000 persons per year. At first sight, such statistics might seem to be of little value (except perhaps to morticians). However, the number of deaths is one indication of the outcome, or impact, of cancer because it represents the product of incidence and the fatality of a given cancer. Fatality, the inverse of survival, is the proportion of cancer patients who die, and this is generally assumed to be the most severe sequel of the disease. Mortality rates therefore measure the average risk to the population of dying of a specific cancer, whereas fatality (defined as 1-survival) represents the probability that an individual with cancer will die of it. Mortality rates are sometimes used as a convenient proxy measure of the risk of acquiring the disease. This use does, however, assume that survival or fatality is constant among the populations being compared. Because this is rarely the case—at least when comparisons are made among countries—it is safer to use mortality as measure of outcome. Prevalence of disease measures the number of persons alive at a particular time who have the disease of concern. Regarding cancer, no clear agreement exists about what is meant by "having" the disease. Some authors take it to mean ever having been diagnosed with cancer, even if this was many years ago, and the subject is cured. This is clearly a useless statistic. Knowing the number of people being treated for cancer (or, at least, still being followed-up medically for the disease) would be more helpful. Such a statistic is not only hard to obtain, but it would certainly vary from one place to another, depending on medical practice. However, since cure is often interpreted as meaning survival beyond 5 years, at least for statistical purposes, a useful compromise is to estimate prevalence as the number of people alive who have had a cancer diagnosed within the last 5 years.1 Several other more complex statistics have been used to measure the impact of disease. They include person-years of life lost (how many years of normal life span are lost because of deaths from cancer) and disability or quality-adjusted life-years lost. The latter measures attempt to give a numerical score to the years lived with a reduced quality of life between diagnosis and death (where quality = 0) or cure (quality = 1). In this article, we present estimates of the incidence of and mortality from cancer, both as numbers of cases and deaths, and as the annual rates of incidence or mortality per 100,000 population. The rates are age-standardized to take into account differences in the age structure of the populations being compared. This is necessary because risk of cancer incidence and mortality is very powerfully determined by age, so that populations containing a high proportion of old people tend to have higher rates than populations with mainly young people. Because we wish to know the risk irrespective of this incidental ("confounding") effect, we compare populations as if they had the same age structure—that of the so-called "world standard population." The ratio of mortality to incidence represents the approximate fatality for a given cancer. A figure of 0.7, for example, means that 70% of patients with new cases will die (or, conversely, that 30% will survive). Because most deaths attributable to cancer occur within 5 years of diagnosis, "survival" as obtained with the formula 1-mortality/incidence is close to the 5-year survival rate obtained by the actual follow-up of groups of new cancer cases.2, 3 Incidence data are available from cancer registries. The number of cancer registries has increased steadily over the years; such registries cover entire national populations or subsamples of selected regions. They also provide statistics on cancer survival, making it possible for incidence to be estimated from mortality. Mortality data by cause are available for many countries because of registration of vital events, although the degree of detail and quality of the data (both the accuracy of the recorded cause of death and the completeness of registration) vary considerably. With such data, estimations of the numbers of new cancer cases and deaths by site, sex, and age group are possible. These estimations are more or less accurate for different countries, depending on the extent and accuracy of locally available data. The most recent comprehensive estimates are for 19904 (also P. Pisani, PhD; D.M. Parkin, MD; F.I. Bray, MSc; and J. Ferlay, International Agency for Research on Cancer [IARC], Lyon, France, unpublished data, 1998). In this paper, these estimates are presented for 23 world "areas" defined by the United Nations (Fig. 1). However, the estimates are built up at country level, and to obtain the full information available, readers should refer to the CD-ROM "GLOBOCAN."5 The information can also be accessed, although with less flexibility in the analyses possible, on the Internet (http://www-dep.iarc.fr/dataava/globocan/globojava.html). Developed countries are areas 10, 12, and 17–21 of Figure 1; developing countries are the remaining areas. This convention is used throughout this article. The terms westernized and industrialized are used as synonyms of developed. No attempt has been made to estimate incidence or mortality of nonmelanoma skin cancer because of the difficulties of measurement and consequent lack of data. The "all cancer" total therefore excludes such tumors. Rates for five broad age groups (0–14, 15–44, 45–54, 55–64, and 65 and over) and sex were estimated for as many individual countries as possible. Age-standardized incidence rates were calculated using the weights of the "world standard" population (0.31, 0.43, 0.11, 0.08, and 0.07) in these five age classes. The area estimates were obtained by combining age- and sex-specific rates for component countries as a weighted average (using the corresponding country populations). 23 World Areas Studied The sources of data for the countries of the 23 world areas and the methods used to produce estimates of incidence and mortality in each of them are summarized in Parkin et al4 and P. Pisani, PhD; D.M. Parkin, MD; F.I. Bray, MSc; and J. Ferlay, IARC, Lyon, France, unpublished data, 1998. In summary, incidence rates for a country were obtained whenever possible from cancer registries serving the whole population or a representative sample of it. In like manner, national mortality data from the World Health Organization (WHO) mortality data bank were used to obtain information on cancer deaths. For some countries, a correction factor was applied to account for known and quantified underreporting of mortality. Occasionally, mortality data from a sample of the country were used in the absence of national statistics. The most prominent example of this was the use of information from disease surveillance points representing a random sample of some 9.6 million (0.8%) of the Chinese population.6 Occasionally, mortality data collected by cancer registries were used. In the absence of either of these data sources, we built up an estimate of cancer incidence from available information on the relative frequency of different cancers (by age group and sex), applied to an overall "all sites" incidence figure for the corresponding area. These "all sites" figures were derived from such data as could be found for the corresponding geographic area. For some countries, data could be found on mortality but not on incidence. In these cases, incidence was estimated using sets of regression models that, for a given area, cancer, and sex and age group, predict incidence from mortality, based on cancer registry data from the same area. The opposite was also true: incidence rates were available for some countries in which no data on mortality existed. For these countries, we used information on cancer survival to obtain estimates of mortality. Three sources of data on population-based survival were used, the Cancer Survival in Developing Countries project by the IARC,7 which provides cancer survival in populations of China, the Philippines, Thailand, India, and Cuba for all of the sites considered; the Surveillance, Epidemiology, and End Results (SEER) program covering 10% of the United States population;8 and the EUROCARE project providing figures from several European cancer registries.9 Table 1 shows population-based relative survival probabilities for the United States (cases diagnosed from 1989 to 19938), Europe,9 China,7 and India,7 and the average survival recorded by ten registries in developing countries (Shanghai and Qidong, China; Barshi, Madras, Bangalore, and Bombay, India; Rizal, Philippines; Chiang Mai and Khon Kaen, Thailand; and Cuba).7 These are the only population-based data available in less affluent countries. For this reason, we take their mean as the best available indication of cancer survival in developing countries, although we recognize that these ten registries are far from a representative sample of the whole region. A thorough discussion of the accuracy and limitations of these data can be found in Sankaranarayanan et al.7 Table 1 also shows estimates of 5-year survival based on the ratio of deaths to cases by geographical region. These estimates of survival are age-adjusted using the age distribution, by site, of worldwide incident cases for males and females combined. Differences between these estimates and the crude rates of the three data sources used in compiling the Table are partly the result of age standardization. The age distribution of patients for any cancer site in developing countries is significantly younger than that of patients in developed countries because of the younger age of the population in developing countries. Standardization of survival rates on the age distribution of world cases (which include those of developing countries) tends therefore to emphasize survival rates of younger patients, which, for several sites, are more favorable. This explains why, for example, the age-adjusted estimated survival from lung cancer in North America is better (20%) than that reported by SEER (14%). The most recent estimate, that for 1990,4 suggests a total of 8.1 million new cases, divided almost exactly between developed and developing countries. This represents an increase of about 37% since our first estimates 15 years ago for 1975, a rate of growth (2.1% per year) that is faster than that of the world population (1.7% per year). In the same year (1990), we estimate that 5.2 million cancer deaths occurred, about 55% of which occurred in developing countries. Table 2 shows the number of new cancers and cancer deaths for 25 sites in males and females and for both sexes combined. Table 3 shows the age-standardized incidence and mortality rates. Incidence and Mortality of the 15 Most Common Cancers in Males Incidence and Mortality of the 15 Most Common Cancers in Females Some differences exist in the profile of cancers worldwide, depending on whether incidence or mortality is the focus of interest. Lung cancer is the main cancer in the world today, whether considered in terms of numbers of cases (1.04 million) or deaths (921,000), because of the high case fatality (the ratio of mortality to incidence is 0:89). Stomach cancer is second in importance (789,000 cases, 628,000 deaths). Although breast cancer is the third most common cancer overall (796,000 new cases), it ranks fifth as a cause of death because of its relatively favorable prognosis (the ratio of mortality to incidence is about 40%). Cancers of the colon and rectum (783,000 cases, 437,000 deaths) and liver (437,000 cases, 427,000 deaths) rank more highly than female breast cancer as cause of death. We gathered breast cancer data for females only. Figure 2 summarizes these results, showing the 15 most common cancers for males and females (as numbers of new cases) and the corresponding numbers of deaths in the developing and developed regions of the world. Table 4 shows the numbers of new cases of and deaths from cancer by world area, and Table 5 shows the corresponding age-standardized rates. The numbers range from 1.4 million cases in China (17% of the world total) and 1.2 million in North America (15%) to about 1,100 in Micronesia/Polynesia. For the world as a whole, the sex ratio (male to female) for cancer deaths is 1.33, which is greater than the sex ratio for incidence (1.13) because of the more favorable prognoses of female cancers. The age-standardized rates in Tables 3 and 5 express the actual risk of developing or dying from cancer, irrespective of the age distribution of the population. Thus, for men the risk of cancer is highest in North America (age-standardized incidence rate 369.9 per 100,000), a consequence, as described later in this article, of the high contemporary rates of prostate cancer. The risk of dying of cancer, in contrast, is highest in Eastern Europe, with an age-standardized incidence rate for all sites of 205 deaths per 100,000 population. Mortality rates in all other developed regions are about 180, although incidence is more variable (260 to 310). In females, the region with the highest incidence of cancer is again North America (age-standardized incidence rate 277.5), whereas mortality is highest in Northern Europe (age-standardized incidence rate 125.4), followed by North America, Southern Africa, and tropical South America. Lung cancer was the most common cancer in 1990, in terms of both incidence (1.04 million new cases; 12.8% of the world total) and mortality (921,000 deaths; 17.8% of the world total); 58% of new cases occur in developed countries. Worldwide, it is by far the most common cancer of men, with the highest rates observed in North America and Europe (especially Eastern Europe). Moderately high rates are also seen in temperate South America, Australia/New Zealand, and parts of Eastern Asia (Fig. 3A, 3B). In females, incidence rates are lower (overall, the rate is 10.8 per 105 women, compared with 37.5 per 105 men). The highest rates are in North America and Northern Europe. The incidence in China is high (age-standardized rate 13.4 per 105), similar to that in, for example, Australia/New Zealand (16.1). Lung cancer remains a highly lethal disease. Survival at 5 years measured by the SEER program in the United States is 14%, the best recorded at the population level. The average survival in Europe is 8%, the same as that of developing countries. The most important cause of lung cancer is tobacco smoking, and incidence rates in a country closely reflec the history of tobacco smoking.10 We have estimated the proportion of lung cancer cases caused by tobacco smoking by examining the observed incidence in different areas compared with that expected based upon incidence rates in nonsmokers from several large cohort studies.11 Incidence of Lung Cancer in Males by World Region Incidence of Lung Cancer in Females by World Region Incidence of Stomach Cancer in Males by World Region Updating the results to 1990, we find that 86% of cases in men and 49% in women are caused by smoking, although considerable regional variation exists in this figure. Thus, in countries or regions with a long history of smoking, 90% or more of cases in men are tobacco related. The fraction is much lower in Africa and Southern Asia. The proportions are more variable in women, even in Europe, where they range from 80% in the United Kingdom to virtually nil in Spain and Portugal, where incidence rates are the same as in nonsmoking women in the United States and Japan. Time trends in lung cancer reflect past exposure to cigarette smoking. Our estimate of the numbers of cases worldwide has increased by 16% since 1985 (an increase of 4% in men and 21% in women). This represents an increase of about 2.5% in the actual risk in men and 9.5% in that in women (the remainder is the result of population growth and aging). The overall upward trend disguises considerable difference among countries. In men, several populations have now passed the peak of the tobacco-related epidemic, and incidence rates are now declining (for example, in the United States and the countries of Northern and Western Europe). In contrast, incidence and mortality are increasing rapidly in Southern and Eastern European countries. In women, the "epidemic" is less advanced. Most western countries are still showing a rising trend in incidence and mortality, although for some there is, so far, no evidence of this (Spain), whereas for others (United Kingdom) the peak of risk now may have been reached. Incidence of Stomach Cancer in Females by World Region Stomach cancer is the second most frequent cancer, with 798,000 new cases (9.9% of the total) and 628,000 deaths (12.1% of cancer deaths), although it is only in fourth rank in women (Fig. 2). Thirty-eight percent of cases occur in China, where it remains the most common cancer in both sexes, as it is elsewhere in Eastern Asia. Age-standardized incidence rates are highest in Japan (77.9 per 100,000 in men, 33.3 per 100,000 in women). High rates are also present in both sexes in Eastern Europe and tropical South America (Fig. 4A, 4B). The rates are low in Eastern and Northern Africa, North America, and South and Southeast Asia (age-standardized incidence rate in men 5.9 to 9.0 per 100,000 and 2.6 to 5.3 per 100,000 in women). Survival for stomach cancer is moderately good only in Japan (53%), where mass screening by photofluoroscopy has been practiced since the 1960s. Other areas with better survival are North America (21% based on the SEER data, 34% age-adjusted estimate) and Australia and New Zealand (29%), possibly because of early diagnosis after a greater number of endoscopic examinations performed for gastric disorders. Survival is 18% on average in European registries and is consistent with the age-adjusted estimates. Elsewhere, survival varies from 10% (Eastern Europe, including Russia) to 21% in Latin America. The differences in risk among countries are usually assumed to be related to dietary factors, which are important in determining the risk of individuals in epidemiologic studies. Their importance is consistent with the descriptive data and studies of migrants. Recently, the importance of Helicobacter pylori has been recognized. The IARC12 has accepted H. pylori as a human carcinogen, based on ecological correlation studies (such as the EUROGAST study13), a host of case-control studies, and, more usefully, several cohort studies. The combined odds ratio from these studies is 2.1.14 H. pylori is assumed to have an indirect action because it provokes gastritis, which is a precursor of gastric atrophy, metaplasia, and dysplasia. The role of dietary and other exogenous factors may be synergistic or antagonistic. Incidence of Breast Cancer in Females by World Region The proportion of the population infected with H. pylori is large in developing countries, ranging from 80% to 90%; individuals contract the infection at a young age, and it persists throughout life. In developed countries, the prevalence is lower. Assuming a value of 50% (and 80% in developing countries) and a relative risk of 2.1, the number of new cases of stomach cancer attributed to the bacterium is 337,800, representing 42% of the world total of these cancers (47% in developing countries and 35% elsewhere). A steady decline has occurred in gastric cancer incidence and mortality in most countries. Our world estimate of the number of new cases in 1990 was just 6% greater than that in 1985, which, given the population increase and aging, represents a decline of 4% to 5% in age-adjusted risk. This decline may be related to improvements in preservation and storage of foods. It also may represent changes in the prevalence of H. pylori by birth cohort, perhaps because of reduced transmission in childhood, following a trend toward improved hygiene and reduction of crowding.15 In any case, one can confidently expect a continuing decline in age-adjusted incidence and mortality from stomach cancer. If the observed rate of decline in the last 5 years continues, the expected number of new cases in 2010 will be about 1 million, an increase of 30% rather than the 58% additional cases resulting simply from population growth and aging. Incidence of Colon and Rectal Cancer in Males by World Region In terms of number of new cases, breast cancer is the third most frequent cancer in the world (796,000 cases in 1990) and by far the most common malignancy of women (21% of all new cases). Worldwide, the ratio of mortality to incidence is about 61%. As a result, breast cancer ranks as the fifth cause of death from cancer overall, although it is still the leading cause of cancer mortality in women (the 314,000 annual deaths represent 14.1% of cancer deaths in females). Incidence rates are high in all of the developed areas (except Japan, where it is third after stomach and colon and rectal cancer), with the highest age-standardized incidence in the United States (87.1 per 100,000) (Fig. 5). The incidence is more modest in North Africa, South America, and Eastern, Southeastern, and Western Asia, but it is still the most common cancer of women in these geographic regions. The rates are low (less than 30 per 100,000) in most of sub-Saharan Africa (except South Africa) and in Asia. The lowest incidence is in China (age-standardized incidence rate 11.8 per 100,000). The prognosis for breast cancer is generally rather good, as illustrated by the survival figures in Table 1. The highest crude survival is reported by the SEER program, 84%, consistent with the age-adjusted estimate for North America of 73%. Survival rates are high in Japan (74%) and Australia/New Zealand (68%) and lower in Europe (53% to 63%, consistent with the EUROCARE crude rate of 67%). Elsewhere survival ranges from 49% to 61%. The prevalence of carriers of the major susceptibility genes (BRCA1 and BRCA2) in the general population is low, and the variation observed among populations (0.05% to 1%) could account for only a small part of the observed international and interethnic variation. Most cases must, therefore, be the consequence of different environmental exposures. Indeed, risk changes markedly after migration, particularly if this takes place at a young age. An important increase occurs among first-, second-, and third-generation Asian migrants to the United States.16 Incidence of Colon and Rectal Cancer in Females by World Region The major influences on breast cancer risk appear to be certain reproductive factors and, less certainly, diet.17 Few attempts have been made, however, to quantify the magnitude of risk differentials among populations, which might be explained by such factors. Incidence rates of breast cancer are increasing in most countries, and the changes are usually greatest in areas where rates were previously low. Since our estimates for 1985, overall incidence rates increased about 0.5% annually (excluding China, where data sources were changed between estimates). At this rate of growth, about 1.35 million new cases would be expected in 2010. However, cancer registries in China are recording annual increases in incidence of more than 5%, and in those elsewhere in Eastern Asia, increases are not much less. Assuming a modest 3% growth in Eastern Asia, the world total in 2010 would be 1.45 million, an 82% increase over the figure for 1990. Colon and rectal cancer accounted for 783,000 new cases in 1990 (9.7% of the world total) and caused 437,000 deaths (8.4% of the world total). Unlike the situation with most sites, incidence and mortality were not much different in males and females (ratio 1.05:1.00). In terms of incidence, colon and rectal cancers rank third in frequency in men and second in women. It is a slightly less prominent cause of mortality (fourth in both sexes because of the relatively favorable prognosis) thanks to the fact that survival is on average better than that of cancer at other, less common sites. Survival at 5 years is 60% as reported by the SEER program; 41% and 42%, respectively, as reported by European and Indian cancer registries; and slightly lower in China and developing countries (32% and 38%, respectively). The lowest estimated survival is in Eastern Europe (30%). Incidence of Liver Cancer in Males by World Region The incidence of colon and rectal cancer is higher in developed countries than in developing countries; the lifetime probability of developing colorectal cancer in developed countries is 4.6% in men and 3.2% in women. The highest incidences are in Australia/New Zealand, North America, and Northern and Western Europe. Moderately high incidence rates are seen in Southern and Eastern Europe and temperate South America. Incidence rates are low in Africa and Asia, except Japan, which now has an incidence equivalent to that in Europe (Fig. 6A, 6B). Colon cancer and rectal cancer are similar in their geographical distribution. However, less variation occurs among countries with rectal cancer than with colon cancer. Thus, in high-risk populations, the ratio of colon cancer to rectal cancer is 2:1 or more (especially in females). In low-risk countries, rates are similar, and in India rectal cancer is even slightly more common. These large geographic differences probably represent the effects of different environmental exposures, presumably mainly dietary. That the risk of colon cancer is quite labile to environmental change has long been evident from migrant studies.18, 19 Now, the rates in Japanese men and women in the United States—at least for colon cancer—exceed those in the white population. The incidence rates of colon cancer have increased in most areas, especially in men, since 1985, although North America is an exception to this trend. Liver cancer is the fifth most important cancer worldwide in terms of numbers of cases (437,000, or 5.4% of new cancer cases) but fourth in terms of mortality (427,000 deaths, 8.2% of the total). This difference reflects the extremely poor prognosis for this cancer; survival rates are 3% to 5% as reported by cancer registries in the United States and developing countries. Consistently low rates are estimated everywhere. Eighty percent of cases (and deaths) are in developing countries. As shown in Figure 7, the areas of high incidence are Western and Central Africa (where liver cancer is responsible for 25% of all cancers in men), Eastern and Southeast Asia, and Melanesia. The incidence is low in developed areas (only in Southern Europe does any substantial risk exist) and in Latin America and South Central Asia. Worldwide, the major risk factors for liver cancer are infection with the hepatitis viruses, hepatitis B and C, and consumption of foods contaminated with aflatoxin. Both viruses confer a 20-fold increased risk of liver cancer.20 Because hepatitis B virus is more prevalent, the distribution of infection worldwide largely explains the patterns of liver cancer. The exception is Japan, where chronic infection with hepatitis B virus is uncommon but where the generations most at risk of liver cancer have a relatively high rate of infection with hepatitis C virus.21 With knowledge of the relative risk and prevalence of infection in different areas, we can estimate the proportion of cases attributable to the two viruses, which is more than 75% of cases worldwide and 85% of cases in developing countries. Here is a powerful case for preventive action. At least for hepatitis B, a vaccine is available, which is effective in preventing infection in childhood. Its success in preventing liver cancer is being formally tested in controlled trials in China and Gambia. Although it will be some time before these trials give the final answer to the question of how much protection vaccination provides, a dramatic demonstration of the results of community vaccination is already available from Taiwan. Here, hepatitis B immunization of newborns was introduced in 1984, and in children 6 to 9 years of age in birth cohorts receiving vaccination, a dramatic decrease in incidence of liver cancer has occurred.22 Prostate cancer is the sixth most common cancer in the world (in terms of number of new cases) and fourth in importance in men. The total annual number of cases is 396,000, which represents 9.2% of cancers in men (14.3% in developed countries and 4.3% in developing countries). It is a less prominent cause of death from cancer, with 165,000 deaths (5.6% of cancer deaths in men, 3.2% of all cancer deaths). The prognosis is relatively good, as reflected by age-adjusted estimates of survival rates (Table 1). More than any other, this is a cancer of the elderly. Thus, in developed countries, 82% of cases occur in men older than 65 years. To place this fact in context, even on a world basis, 81% of cases occur in the elderly. Incidence rates are now influenced by the diagnosis of latent cancers found during the screening of asymptomatic individuals. In areas where this practice is common, the "incidence" may be very high (95.1 per 100,000 in the United States, for example, where it is now by far the most commonly diagnosed cancer in men). Inciden